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Efficiency of Semen Cryopreservation in Stallions

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Efficiency of Semen Cryopreservation in Stallions animals Article Efficiency of Semen Cryopreservation in Stallions Jörg Aurich 1, Juliane Kuhl 2, Alexander Tichy 3 and Christine Aurich 2,* 1 Obstetrics, Gynaecology and Andrology, Department for Small Animals and Horses, Vetmeduni Vienna, 1210 Vienna, Austria; [email protected] 2 Artificial Insemination and Embryo Transfer, Department for Small Animals and Horses, Vetmeduni Vienna, 1210 Vienna, Austria; [email protected] 3 Bioinformatics and Biostatistics, Department for Biomedical Science, Vetmeduni Vienna, 1210 Vienna, Austria; [email protected] * Correspondence: [email protected] Received: 20 May 2020; Accepted: 10 June 2020; Published: 13 June 2020 Simple Summary: The quality of stallion semen after freezing and thawing differs among stallions, but it remains to be determined whether such differences are also affected by horse breed. In this study, semen quality was analysed retrospectively in 1012 frozen–thawed ejaculates from 134 stallions of 5 breeds. The percentage of ejaculates acceptable for artificial insemination (AI) and the number of insemination doses per ejaculate was then calculated. Sperm motility before freezing was the most important explanatory variable for the percentage of ejaculates with a post-thaw quality acceptable for AI. Of the other variables studied, stallion age was the most important parameter and a decrease in the percentage of acceptable ejaculates was evident in stallions older than 9 years. There were also more acceptable frozen–thawed ejaculates in Arab stallions compared to Warmbloods, Quarter Horses and Icelandic horses. The analysis thus demonstrates differences in the percentage of acceptable cryopreserved ejaculates among breeds. Total sperm count was the most important variable determining the number of semen doses obtained per acceptable frozen–thawed ejaculate. Abstract: Differences in the cryotolerance of spermatozoa exist among stallions, but it remains to be determined to what extent such differences are affected by breed. In this study, post-thaw semen quality in stallions presented for semen cryopreservation was analysed retrospectively (1012 ejaculates from 134 stallions of 5 breeds). The percentage of frozen–thawed ejaculates acceptable for artificial insemination (AI) and the number of insemination doses per cryopreserved ejaculate was calculated. Logistic regression analysis revealed sperm motility in raw semen as the most important explanatory variable for the percentage of cryopreserved ejaculates with a post-thaw quality acceptable for AI. Of the other variables included into the model, stallion age was the most important parameter with more acceptable ejaculates in younger than in older stallions. Logistic regression also showed more acceptable frozen–thawed ejaculates in Arab stallions versus Warmbloods, Quarter Horses and Icelandic horses. The analysis thus demonstrates differences in the percentage of acceptable cryopreserved ejaculates among horse breeds. Season was a less relevant explanatory variable for percentage of acceptable cryopreserved ejaculates. Logistic regression revealed total sperm count as the most important variable determining the number of cryopreserved semen doses obtained per acceptable ejaculate. In conclusion, logistic regression analysis revealed stallion age and breed as explanatory variables for the percentage of cryopreserved ejaculates acceptable for AI. Keywords: breed; cryopreservation; horse; semen Animals 2020, 10, 1033; doi:10.3390/ani10061033 www.mdpi.com/journal/animals Animals 2020, 10, 1033 2 of 13 1. Introduction In equine artificial insemination (AI), cryopreserved semen is used far less frequently than fresh or cooled-stored semen [1,2]. This is at least in part due to differences in the fertilizing capacity of frozen–thawed semen among stallions [3–6]. Furthermore, cryopreservation of semen is associated with substantial costs. The number of insemination doses obtained per ejaculate thus contributes to the economic efficiency of commercial AI with cryopreserved semen. The efficiency of semen cryopreservation in commercial equine AI programs has not, to the best of our knowledge, been investigated so far. Differences in the number of cryopreserved insemination doses per ejaculate exist among individual stallions, but it remains to be determined whether such differences are also affected by horse breed. Although semen has been frozen from a large number of breeds, ranging from draught horses [7] to Shetland ponies [8,9], differences among horse breeds in post-thaw motility and sperm DNA fragmentation have only recently been investigated in one study [10]. In that study, except for a slightly lower sperm DNA fragmentation in semen frozen from Arab compared to Thoroughbred stallions, post-thaw semen quality did not differ among Arab, Thoroughbred and Warmblood stallions. To the best of our knowledge, the efficiency of semen cryopreservation, i.e., the percentage of frozen–thawed ejaculates classified as acceptable for commercial AI and the number of insemination doses obtained per ejaculate, have not been analysed when using the same cryopreservation protocol in different breeds. However, this is of increasing interest as AI with cryopreserved semen is becoming an alternative in more and more horse breed registries. Under commercial conditions, the number of cryopreserved semen doses per ejaculate is of great interest, provided post-thaw semen quality is of acceptable quality. Preliminary data from our group indicate that the production of cryopreserved semen in horses might be most efficient during the summer months [11,12]. Seminal plasma affects the quality of cryopreserved stallion semen [5]. Seasonal variations in seminal plasma composition may therefore contribute to changes in the quality of processed semen. Additionally, seasonal changes in the composition of the equine sperm plasma membrane have to be considered [13]. Stallions reach their full spermatogenetic capacity not before an age of six years [14] and, furthermore, post-thaw sperm motility was lower in stallions up to six years of age than in older stallions [10]. Additionally, in cattle, total sperm motility, membrane integrity and concentration of motile spermatozoa determined after freezing-thawing were higher in 4-year-old than in yearling bulls [15]. In sheep, frozen–thawed semen from mature rams had less hyperactivated and peroxidised spermatozoa and higher percentages of viable non-capacitated spermatozoa, spermatozoa with an intact plasma membrane, functional mitochondria and condensed chromatin than frozen–thawed semen from young rams. Consequently, lambing rate was higher in ewes inseminated with frozen–thawed semen from mature versus young rams [16]. In the present study, we have retrospectively analysed post-thaw semen quality in stallions admitted to the Centre for Artificial Insemination and Embryo Transfer at Vetmeduni Vienna for semen cryopreservation. The percentage of frozen–thawed ejaculates meeting recommendations for commercial use in equine AI and the number of insemination doses obtained per cryopreserved ejaculate was then calculated. We hypothesized that the percentage of acceptable frozen ejaculates and thus the economic efficiency of equine semen cryopreservation depends on breed of the stallion, increases with age of the stallion until sexual maturity and differs among ejaculates frozen at different times of the year. Classification and regression trees (CART) analysis was used for determination of a relationship between the percentage of ejaculates acceptable for AI and age and breed of stallion as well as season. Classification and regression trees are a nonparametric method used to explain the variation in a response variable with one or more explanatory variables. The analysis separates the response variable into two groups based on one of the explanatory variables. Further splits are obtained in the same way within each of the first two groups [17]. Furthermore, the individual stallion and pre-freeze semen motility were analysed as explanatory variables. Animals 2020, 10, 1033 3 of 13 2. Materials and Methods 2.1. Animals Semen characteristics in raw, diluted and frozen–thawed semen from ejaculates (n = 1221) collected from 164 stallions referred to the Centre for Artificial Insemination and Embryo Transfer of Vetmeduni Vienna between 2004 and 2016 were analysed retrospectively. All stallions underwent a breeding soundness examination before and were only included into the cryopreservation programme when raw semen characteristics at this examination met minimal requirements (>70% motile spermatozoa, sperm concentration >100 106/mL, total sperm count >5 109). Semen was cryopreserved following × × European Union regulations (Directive 65/92 EEC) and stallions were therefore tested serologically negative for equine infectious anaemia and negative for contagious equine metritis based on PCR performed on two sets of penile swabs collected at a 7 day-interval. Stallions were either serologically negative for equine viral arteritis or were tested as not shedding equine arteritis virus in their semen. Decisions on the number of ejaculates and/or insemination doses to be frozen were made by the owner of the individual stallion. Only breeds with more than seven stallions were included into the analysis, leaving 1012 ejaculates from 134 stallions and five breeds. The breeds, number of stallions and number of ejaculates included in the study are summarised in Tables1 and2. Ejaculates were grouped according to the stallion’s
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